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AJR.17.18749

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Wo m e n ’s I m a g i n g • C l i n i c a l Pe r s p e c t i ve
Covington et al.
Future of Contrast-Enhanced Mammography
FOCUS ON:
Downloaded from www.ajronline.org by Kings College London on 10/25/17 from IP address 137.73.144.138. Copyright ARRS. For personal use only; all rights reserved
Women’s Imaging
Clinical Perspective
Matthew F. Covington1,2
Victor J. Pizzitola1
Roxanne Lorans1
Barbara A. Pockaj 3
Donald W. Northfelt 4
Catherine M. Appleton2
Bhavika K. Patel1
Covington MF, Pizzitola VJ, Lorans R, et al.
Keywords: contrast-enhanced digital mammography,
contrast-enhanced mammography, contrast-enhanced
spectral mammography
doi.org/10.2214/AJR.17.18749
Received July 11, 2017; accepted after revision
September 5, 2017.
Based on a presentation at the Society of Breast Imaging
2017 annual meeting, Los Angeles, CA.
1
Department of Radiology, Mayo Clinic, Scottsdale, AZ.
2
Department of Radiology, Mallinckrodt Institute of
Radiology, Washington University in St. Louis,
510 South Kingshighway Blvd, St. Louis, MO 63110.
Address correspondence to M. F. Covington
(covington@wustl.edu).
3
Department of General Surgery, Mayo Clinic,
Scottsdale, AZ.
4
Department of Oncology, Mayo Clinic, Scottsdale, AZ.
AJR 2018; 210:1–9
0361–803X/18/2102–1
© American Roentgen Ray Society
The Future of Contrast-Enhanced
Mammography
OBJECTIVE. The purpose of this article is to discuss facilitators of and barriers to future
implementation of contrast-enhanced mammography (CEM) in the United States.
CONCLUSION. CEM provides low-energy 2D mammographic images analogous to digital mammography and contrast-enhanced recombined images that allow assessment of neovascularity similar to that offered by MRI. The utilization of CEM in the United States is currently
low but could increase rapidly given the many potential indications for its clinical use.
ontrast-enhanced mammography (CEM) is an emerging breast
imaging technique that uses contrast-enhanced recombined images for assessment of neovascularity similar
to MRI [1–7]. CEM is currently available at a
small number of breast imaging centers. The
low rate of adoption of CEM may result from
a lack of familiarity with this technology and
uncertainty regarding how to incorporate
CEM into existing breast imaging practices.
Since its implementation of CEM in 2015,
Mayo Clinic in Arizona has performed approximately 700 CEM examinations. Technical details regarding the acquisition of
CEM images at Mayo Clinic in Arizona have
been previously published elsewhere [2, 3, 8].
The purpose of this article is to present an
overview of CEM specifically pertaining to
the implementation and future use of CEM
in the United States.
C
Facilitators of Implementation
Contrast-Enhanced Mammography Image
Acquisition and Interpretation
CEM takes approximately 8–10 minutes
to perform and provides four low-energy
views analogous to those obtained with 2D
full-field digital mammography (FFDM) as
well as four contrast-enhanced recombined
images obtained after IV administration
of iodinated contrast material (iohexol, 1.5
mL/kg [Omnipaque 350, GE Healthcare])
at a rate of 3 mL/s, with an optimal imaging
window of 2–6 minutes after contrast injection. The recombined images show regions
of contrast enhancement while subtracting
the background breast parenchyma, similar
to contrast-enhanced subtraction breast MRI
(Fig. 1). Like conventional mammography
images, CEM images are acquired in craniocaudal and mediolateral oblique views. Other diagnostic mammography views may also
be obtained if acquired within 8–10 minutes after contrast injection to avoid contrast
washout from the breast [9]. To breast imagers, CEM images look familiar and may be
faster to interpret than MR images, with a
mean total image interpretation time of 1–2
minutes noted at Mayo Clinic in Arizona [8].
Potential Use of Contrast-Enhanced
Mammography for Supplemental Screening
Use of CEM for supplemental screening
may benefit women with an intermediate to
high lifetime risk of breast cancer, including
women with dense breast tissue. Initial studies suggest that, for dense breast tissue, CEM
performs better than 2D mammography for
detecting malignancy and avoiding falsenegative results [5, 10–12] (Fig. 2).
Breast MRI currently provides the highest
sensitivity for detection of malignancy and
provides higher cancer detection yields for
supplemental screening than do molecular
breast imaging, screening breast ultrasound,
and tomosynthesis [13]. However, MRI is
only cost-effective for supplemental screening of women with a lifetime risk of breast
cancer greater than 20%, such as women
with BRCA1 or BRCA2 genetic mutations
[13–15]. The sensitivity of CEM for cancer
detection may approximate that of MRI [1,
4–6, 16]. Data from Mayo Clinic in Arizo-
AJR:210, February 20181
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Covington et al.
na show that CEM may be performed at approximately 25% of the cost of MRI [8]. This
lower cost could facilitate cost-effective supplemental screening for women with an intermediate lifetime risk of malignancy, such
as women with dense breast tissue.
CEM could hypothetically be performed
as both the primary and supplemental screening examination for women with dense breast
tissue, given that CEM provides low-energy 2D images analogous to those from 2D
FFDM (the primary screening examination)
as well as contrast-enhanced recombined
images (the supplemental screening examination), which may be unaffected by dense
breast tissue [8, 17]. It is possible that 2D
FFDM with tomosynthesis (or tomosynthesis
with a synthesized 2D image) could also constitute the primary and supplemental screening examinations, respectively, although, for
tomosynthesis, the supplemental cancer detection rate in dense breast tissue is relatively
low (1.3 cancers per 1000 women who undergo screening) [13, 18]. Future CEM systems
may use contrast-enhanced tomosynthesis,
although the advantage of using these systems requires further study [16, 19].
Constrast-Enhanced Mammography Use in the
Diagnostic Setting
From a review of clinical contrast-enhanced digital mammography cases at Mayo
Clinic in Arizona, most CEM examinations
have been performed to evaluate abnormal findings on screening mammography
(39.8%), determine the extent of disease for
presurgical planning or response to neoadjuvant therapy (24.8%), and assess clinically detected breast abnormalities (23.1%) (Fig.
3). These data are illustrative only and do not
represent proof of efficacy of CEM for these
indications, although published research
from our institution and others has shown favorable results for a variety of clinical indications [1–11, 20]. Note that CEM is typically performed at Mayo Clinic in Arizona as
a supplement to MRI for the assessment of
response to neoadjuvant therapy, for which
MRI is considered the reference standard;
however, it is often performed in place of
MRI for other indications, such as the evaluation of abnormal findings on screening mammography. In addition, CEM is approved by
the U.S. Food and Drug Administration and
is available for clinical use at Mayo Clinic
in Arizona, similar to mammography, breast
ultrasound, and breast MRI. Informed consent is not routinely obtained at Mayo Clinic
2
in Arizona for CEM or contrast administration, similar to contrast-enhanced CT, unless
imaging is specifically performed as part of
a research protocol.
Substitute Contrast-Enhanced Breast Imaging
Modality for Those With Contraindications to
Breast MRI
CEM is particularly useful for patients with
claustrophobia, leading to higher satisfaction
among patients and referring clinicians when
compared with MRI [21]. CEM may also be
beneficial for patients who cannot complete
MRI because of body habitus, table weight
limits, or other contraindications to MRI, such
as the presence of pacemakers. Advantages of
CEM compared with MRI include greater
ease of scheduling, faster imaging and interpretation times, and improved patient comfort
given no claustrophobia [2, 8].
Because CEM provides rapid contrastenhanced imaging, CEM may be added to a
full breast imaging schedule at Mayo Clinic
in Arizona with little disruption, similar to
breast ultrasound. At Mayo Clinic in Arizona, CEM can often be performed, and images interpreted, within 30–60 minutes of the
study being requested by the referring provider. For example, if the extent of disease
is unclear after diagnostic mammography,
ultrasound, or both, CEM may be added in
real-time, which may obviate MRI. Alternatively, at our institution, clinicians from the
breast clinic (located in close proximity to
the breast imaging center) may request an
add-on CEM examination to be performed at
the time of a patient’s clinical appointment,
for any concern not explained on prior mammography or ultrasound (Fig. 4).
Potential Barriers to Implementation
Iodinated Contrast Exposure
Risks of CEM include patient exposure to
iodinated contrast materials. Although inherent risks from this exposure are thought
to be extremely small, these risks nevertheless may limit the use of CEM for supplemental screening.
Severe hypersensitivity reactions to lowosmolality iodinated contrast media are
thought to occur in up to four in 10,000 administrations, with the possibility of death
occurring in one in 100,000–170,000 administrations [22–25], although a single large
Japanese study noted no fatal reactions resulting from greater than 170,000 injections
[26]. Therefore, a range of zero to 10 deaths
due to hypersensitivity reactions are antici-
pated per every million women undergoing
CEM (or any other examination with low-osmolality iodinated contrast material).
When it is considered that up to 50% of
women aged 40–59 have dense breasts and
approximately half of the 43 million women
in this age range in the United States complete
mammographic screening, approximately 20
million women with dense breast tissue could
be considered for supplemental screening [27,
28]. The cumulative number of serious or fatal hypersensitivity reactions that would be
expected to occur if these women completed
CEM is small but not inconsequential.
Contrast-induced nephropathy may also
result from exposure to iodinated contrast
material [22]. Assuring that the patient has
adequate renal function before CEM is performed adds cost and requires technologist
support, nursing support, or both, similar to
contrast-enhanced CT.
Ionizing Radiation Exposure
CEM has theoretic risks from ionizing radiation exposure that may limit its use, despite these risks being extremely small or
nonexistent [29]. For CEM, mean glandular
dose estimates vary according to breast density and are estimated to be 20–80% higher than those associated with standard 2D
FFDM alone but lower than those associated
with a standard 2D FFDM plus 3D mammography [30–33]. For CEM, the mean glandular
dose for all breast tissue compositions ranges
from 1.1 to 2.8 mGy [31, 32], compared with
0.5 mGy for molecular breast imaging [34].
However, molecular breast imaging has additional systemic radiation exposure, including a colonic absorbed dose of 11–15 mGy
[34]. Although ultrasound and MRI do not
use ionizing radiation, these technologies often require initial mammography with corresponding radiation exposure.
Like MRI, CEM may also depict background enhancement resulting in false-positive results requiring additional workup. To
minimize this risk, CEM is best performed
in the luteal phase of the menstrual cycle.
Also similar to breast MRI, CEM may show
enhancement of benign breast masses like fibroadenomas or papillomas, which can lead
to false-positive breast biopsy recommendations for otherwise benign masses, although
the rate of false-positive results from CEM
may be less than that from MRI [1], with a
similar overall specificity [1, 5, 8].
MRI remains the reference standard for
supplemental screening of women with
AJR:210, February 2018
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Future of Contrast-Enhanced Mammography
a high (> 20%) lifetime risk of breast cancer in accordance with current American
Cancer Society guidelines [35]. Therefore,
CEM may be an ideal alternative for women with an intermediate risk of breast cancer who may not be eligible for supplemental
screening MRI. Multicenter trials that compare CEM with tomosynthesis and emerging
technologies, including automated wholebreast ultrasound, molecular breast imaging,
and abbreviated MRI, are needed.
Limited FOV Compared With MRI
Given its smaller FOV, CEM is also expected to be inferior to MRI for the detection of chest wall invasion, internal mammary metastasis, and, potentially, axillary nodal
disease in patients with known breast cancer.
Personnel Requirements for ContrastEnhanced Mammography
Similar to contrast-enhanced CT, CEM
requires placement of an IV line and evaluation of renal function before imaging, as well
as monitoring for potential contrast reactions
after imaging. These tasks may be performed
by either mammography technologists or
nurses. A radiologist or other licensed physician must be physically present during CEM
imaging to evaluate and treat any contrastassociated reaction. In addition, determination of previous contrast reactions and adequate renal function needs to be performed,
which again is similar to requirement for
contrast-enhanced CT. CEM images are obtained by mammography technologists using
standard mammography positioning. It is estimated that the personnel expense associated with CEM is approximately 60% lower
than that associated with MRI [8].
Contrast-Enhanced Mammography
Implementation
Implementation of CEM into a breast imaging practice may be favorable in terms of
equipment acquisition costs and space allocation needs because current-generation mammography systems are frequently delivered
with CEM capability. U.S. Food and Drug
Administration–approved contrast-enhanced
mammography systems include the SenoBright system (GE Healthcare), approved in
2011 and often known as contrast-enhanced
spectral mammography, and the Selenia Dimensions system (Hologic), approved in 2013
and often known as contrast-enhanced digital
mammography. For practices that own mammography systems with CEM capability, im-
plementation would require the purchase of
a software upgrade from the vendor, insertion of a copper filter into the existing mammography unit, and acquisition of a standard
contrast power injector [8]. CEM may then
be performed in the existing mammography suite, precluding the need for additional space. For such practices, acquisition costs
and space requirements associated with CEM
will be favorable compared with alternatives
like MRI, automated whole-breast ultrasound, and molecular breast imaging.
CEM acquisition costs will be higher
for practices that do not own CEM-capable
mammography systems. However, implementation of CEM for these practices may
still be favorable given that CEM-capable
mammography systems can perform standard 2D and 3D mammography as well as
stereotactic 2D-guided procedures, 3D-guided procedures, or both (depending on the vendor and equipment upgrades). This versatility
provides operational flexibility and multiple
potential revenue streams to offset CEM acquisition and installation costs. Although uncertain, adoption of CEM into imaging practices in the United States could potentially be
rapid given the increasing number of practices that use CEM-capable mammography
units, requiring only minor modifications of
existing equipment to obtain full CEM capability. Furthermore, CEM was implemented
at Mayo Clinic in Arizona by existing mammography technologists who were trained to
perform CEM, and there was no need to hire
additional technologists. Nursing support
may be beneficial for placement of the IV line
and assistance with management of contrast
reactions, so a dedicated nurse was hired for
this purpose at Mayo Clinic in Arizona.
CEM adoption faces significant competition from breast MRI and other emerging
breast imaging technologies. Many breast
imaging practices in the United States have
invested significant resources to acquire and
maintain breast MRI systems. These practices may be reluctant to invest additional resources to acquire CEM.
Unlike MRI, CEM has no commercially
available system to biopsy regions of suspicious enhancement under CEM guidance [3,
9]. A method was developed at Mayo Clinic
in Arizona to place a clip or seed at a site
of suspicious enhancement, with the use of
CEM guidance for subsequent stereotactic core needle biopsy or surgical excisional biopsy targeting the clip or seed (Fig. 5).
However, this requires that two procedures
be performed—CEM clip or seed placement
followed by stereotactic-guided biopsy—to
obtain tissue samples. To our knowledge, it is
unclear whether a commercial CEM–guided
biopsy system will become available.
Economic Considerations for
Contrast-Enhanced Mammography
Implementation and Future Use
Future use of CEM in the United States
will be affected by health care payment models and examination-specific reimbursement
levels. Current fee-for-service payment models incentivize practices to use MRI rather
than CEM given current higher reimbursement for breast MRI. However, if alternative
payment models were implemented to incentivize lower imaging expenditures, such as
bundled payments for episodes of care, CEM
would then be favored.
Data from Mayo Clinic in Arizona show
that CEM is currently performed at approximately 25% of the cost of MRI and that, depending on the state or region, CEM may be
reimbursed as the cost of diagnostic mammography plus the cost of iodinated contrast
materials [8]. Using CEM as an alternative
to MRI could lower overall imaging costs to
the health care system by more than 1 billion
U.S. dollars annually [8].
If CEM were used as an alternative to
MRI, imaging practices that heavily rely on
MRI revenue may face financial declines.
Alternatively, CEM could potentially allow
cost-effective supplemental screening for
subgroups of women for whom MRI is currently cost-prohibitive, such as women with
an intermediate risk of breast cancer, thereby
potentially increasing imaging volumes and
creating new sources of revenue. Data from
Mayo Clinic in Arizona suggest that CEM
is also faster to perform and interpret and
has lower equipment acquisition and maintenance costs than does MRI [8].
CEM will compete for future reimbursement with other emerging breast imaging
modalities, including abbreviated breast
MRI, molecular breast imaging, positronemission mammography, PET/MRI, contrast-enhanced breast ultrasound, automated
whole-breast ultrasound, and breast CT with
or without contrast enhancement. If value is
defined as health outcomes achieved per dollar spent [36], CEM is likely to be among the
propositions offering the best value in comparison with other emerging imaging technologies, particularly if reimbursement for
CEM remains at or below current levels.
AJR:210, February 20183
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Summary
The initial experience with clinical CEM
use at Mayo Clinic in Arizona shows that this
technology allows imaging practices to perform rapid contrast-enhanced imaging of the
breast with lower imaging costs and shorter
imaging and interpretation times than breast
MRI. Given the growing body of evidence
supporting CEM use for various clinical indications, CEM should be considered for expanded clinical use at other breast imaging
centers in the near future. The drawbacks of
CEM include patient exposure to iodinated
contrast materials with low risks of contrastinduced reactions and theoretic risks from
radiation exposure. Although CEM is currently available at a minority of breast imaging practices, widespread adoption could
be rapid given that many current-generation
mammography systems are delivered capable of use for CEM. Expanded CEM use will
be impacted by payment models and future
research on CEM as an adjunct or alternative to mammography, ultrasound, MRI, or a
combination of these modalities.
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Future of Contrast-Enhanced Mammography
Fig. 1—44-year-old woman with invasive ductal
carcinoma of left breast.
A, Low-energy craniocaudal (top) and mediolateral
oblique (bottom) images from contrast-enhanced
mammography (CEM) appear analogous to standard
2D digital mammographic views and show large
spiculated mass (arrows) in upper outer left breast.
B, Recombined (subtraction) CEM images show
heterogeneously enhancing irregular mass in
upper outer left breast on craniocaudal (top) and
mediolateral oblique (bottom) views.
C, Fat-suppressed delayed contrast-enhanced
T1-weighted axial MR image of left breast shows
heterogeneously enhancing irregular mass in upper
outer left breast.
D, Contrast-enhanced sagittal subtraction MR image
appears most similar to recombined CEM views
and shows heterogeneously enhancing irregular
mass in upper outer left breast, analogous to CEM
recombined images.
A
B
C
D
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Covington et al.
A
B
C
Fig. 2—45-year-old woman with heterogeneously dense breast tissue.
A, Images from completed screening mammography craniocaudal views (top) and mediolateral oblique views (bottom) show 1.1-cm mass (circle) in central right breast.
This mass persisted on diagnostic spot compression tomosynthesis views and was circumscribed and hypoechoic on targeted ultrasound (images not shown). Six-month
follow-up imaging was recommended for probably benign fibroadenoma. Given her dense breast tissue, patient completed supplemental screening 1 week later with lowdose molecular breast imaging, which showed focal intense radiotracer uptake in upper outer left breast with no concerning uptake in right breast (images not shown).
Left breast spot compression tomosynthesis views (not shown) showed 1-cm mass with indistinct margins.
B, Targeted ultrasound image shows round 1-cm irregular mass with indistinct margins. Ultrasound-guided biopsy revealed invasive ductal carcinoma.
C, Recombined postcontrast craniocaudal (top) and mediolateral oblique (bottom) views from contrast-enhanced mammography obtained for presurgical planning show
enhancing 1.2-cm mass in upper outer left breast with no suspicious enhancement in right breast (arrow), corresponding with findings on molecular breast imaging.
Breast conservation therapy was offered, but patient elected to undergo bilateral mastectomy. Final surgical pathologic analysis revealed presence of invasive ductal
carcinoma of left breast with lobular features and benign apocrine metaplasia and nonproliferative fibrocystic changes in right breast.
0
50
100
150
200
250
300
Abnormal finding on screening mammogram
Presurgical evaluation or neoadjuvant response
Clinically detected breast abnormality
Post-lumpectomy surveillance
High-risk screening
Assessment of complicated imaging
BI-RADS category 3
Dense breast supplemental screening
Evaluation of radiologic-pathologic discordance
6
Fig. 3—Indications for which contrast-enhanced
mammography (CEM) was performed for first 605
cases. Data are number of CEM cases.
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Future of Contrast-Enhanced Mammography
Fig. 4—45-year-old woman with physician-detected
right upper outer breast palpable concern 2 weeks
after screening mammography.
A, Screening craniocaudal (above) and mediolateral
oblique (below) mammograms show dense breast
tissue but was otherwise reported to be normal.
Patient was referred to breast clinic where right
upper outer palpable concern was confirmed
by breast surgeon, who then ordered contrastenhanced mammography (CEM), which was
completed at patient’s appointment.
B, Recombined postcontrast CEM craniocaudal
(above) and mediolateral oblique (below) views
showed large area of nonmass enhancement
(arrows) in superior right breast and enhancing
6-mm focus (arrowhead) in left upper outer breast.
CEM-directed ultrasound showed ill-defined
mixed-echogenicity indistinct mass in upper right
breast and no sonographic finding in left breast
(images not shown). Ultrasound-guided right breast
biopsy revealed invasive lobular carcinoma. Spot
compression tomosynthesis views of left upper outer
breast showed circumscribed 6-mm mass, which
was stable on 6-month follow-up spot compression
tomosynthesis views (images not shown).
A
B
A
B
C
Fig. 5—Images of method used to place a clip or seed at site of suspicious enhancement, with contrast-enhanced mammography used for guidance for subsequent
stereotactic core needle biopsy or surgical excisional biopsy targeting the clip or seed.
A–F, Recombined postcontrast contrast-enhanced mammography (CEM) images of breast. Lateral view obtained 2 minutes after contrast administration show that
abnormal area of enhancement to be targeted (arrow, A) is adequately positioned under localization grid. Other lateral view shows biopsy clip needle in good position
(B), subsequent orthogonal craniocaudal view shows tip of needle just beyond area of enhancement (C). Remaining craniocaudal views show that slight retraction tip of
needle is located at edge of enhancement (D) and deployment of ribbon biopsy clip at targeted area of suspicious enhancement (E and F).
(Fig. 5 continues on next page)
AJR:210, February 20187
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Covington et al.
D
E
F
G
H
I
Fig. 5 (continued)—Images of method used to place a clip or seed at site of suspicious enhancement, with contrast-enhanced mammography used for guidance for
subsequent stereotactic core needle biopsy or surgical excisional biopsy targeting the clip or seed.
A–F, Recombined postcontrast contrast-enhanced mammography (CEM) images of breast. Lateral view obtained 2 minutes after contrast administration show that
abnormal area of enhancement to be targeted (arrow, A) is adequately positioned under localization grid. Other lateral view shows biopsy clip needle in good position
(B), subsequent orthogonal craniocaudal view shows tip of needle just beyond area of enhancement (C). Remaining craniocaudal views show that slight retraction tip of
needle is located at edge of enhancement (D) and deployment of ribbon biopsy clip at targeted area of suspicious enhancement (arrow) (E and F).
G and H, Paired stereotactic images following firing of biopsy needle show biopsy needle targeting ribbon-shaped clip placed under contrast-enhanced mammography guidance.
I, Specimen radiograph from stereotactic-guided biopsy shows removal of clip.
(Fig. 5 continues on next page)
8
AJR:210, February 2018
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Future of Contrast-Enhanced Mammography
Fig. 5 (continued)—Images of method used to place
a clip or seed at site of suspicious enhancement, with
contrast-enhanced mammography used for guidance
for subsequent stereotactic core needle biopsy or
surgical excisional biopsy targeting the clip or seed.
J, Lateral mammogram shows deployment of new
bar-shaped clip to mark site of stereotactic-guided
core needle biopsy.
K, Lateral mammogram obtained after stereotactic
vacuum-assisted core biopsy shows removal of
ribbon clip and placement of bar-shaped clip (circle)
that closely corresponds to region of enhancement
on initial digital subtraction image (A). Pathologic
findings from stereotactic core biopsy showed
complex sclerosing lesion with ductal carcinoma in
situ.
J
K
AJR:210, February 20189
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